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The Shape of Fungal Ecology: Does Spore Morphology Give Clues to a Species’ Niche?

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The Shape of Fungal Ecology: Does Spore Morphology Give Clues to a Species’ Niche? fungal ecology 17 (2015) 213e216 available at www.sciencedirect.com ScienceDirect journal homepage: www.elsevier.com/locate/funeco Commentary The shape of fungal ecology: does spore morphology give clues to a species’ niche? Pick up any botany textbook, and you can read about the the spore of a saprotrophic Amanita look somehow con- morphologies of flowers: “most bird flowers are colorful, with sistently different from the spore of a mycorrhizal Amanita? red and yellow ones being the most common. bat flowers are While many modern fungal ecologists may eschew the typically dully colored, and many of them open only at night” study of spores and sporocarps as throwbacks to a pre- (Raven et al., 1992 pp. 424e425). The color, smell, and shape of molecular era, Peay (2014), Halbwachs et al. (2015) and a flower (as well as quality of nectar and phenology) are used Bassler€ et al. (2014) ask whether there are predictable differ- to predict the kind of pollinator associated with a species. For ences between the spores and sporocarps of saprotrophic and example, red flowers that do not smell but produce high ectomycorrhizal fungi. Among other results, Bassler€ et al. quality nectar are associated with hummingbirds, which is (2014) found that saprotrophic fungi produce smaller spor- why hummingbird feeders are often brightly colored and filled ocarps than ectomycorrhizal species, and Halbwachs et al. with strong sugar water. Morphology can be manipulated to (2015) found that spores of ectomycorrhizal species are more attract specific pollinators, and pollination syndromes are likely to be ornamented. There are a number of challenges to commonly discussed in the literature (Rosas-Guerrero et al., these kinds of analyses e including, trophic status and spore 2014). Seeds are also a clue to ecology, for example, plants morphology are influenced by phylogeny, and estimating making copious numbers of very small, light, seeds, are likely independent changes in either character requires phyloge- to use wind as a dispersal vector; seeds with elaiosomes are netically explicit statistical models. Meerts (1999) used phy- likely to be dispersed by ants (Raven et al., 1992). logenetically independent contrasts to demonstrate lineage What about a spore that is ornamented? Can a mycologist specific differences in correlations of spore and sporocarp know anything about ecology from looking at the shape (Roper sizes. In some cases correlations were positive (for example, et al., 2008) or size of a spore, or the size or phenology of a in Agaricus and Coprinus) while in other cases, correlations sporocarp? Obviously, morphology is a clue to taxonomy; were negative (Psathyrella). While Halbwachs et al. (2015) and ascospores look different from basidiospores. A spore of a Bassler€ et al. (2014) attempt to control for phylogenetic inter- Cordyceps looks like nothing else. dependence, there are reasons to query their assumptions and But perhaps morphology can offer more. The effective methods. For example, the species included in analyses do not dispersal of spores plays an essential role in the ability of fungi form a monophyletic group, although they are treated as a to reach and colonize new substrata. Many spore features are single group, and ancestral state analyses of nutritional mode likely to be under adaptive selective pressures related to the and spore surface characters are not provided. In addition, the particular ecological niche of a species. In fact, the morpho- species are taken from a single geographic region (Northern logical diversity of spores and the sporocarps holding them is Europe), and may be dominated by particular subsets of fungal astonishing (Pringle, 2013), and begs for explanation. In some diversity, including ectomycorrhizal Cortinarius species with cases, morphological diversity is easily explained, for exam- ornamented spores. Nonetheless, both articles ask questions ple, the characteristic forms of hypogeous truffles are the worth thinking about, and provide a valuable path forward. result of natural selection for animal dispersal, and so hypo- If these findings hold, what can they teach us about the geous basidiomycete truffles lack functional sterigmata. selective pressures experienced by fungi in different niches? Understanding these morphologies provides clues in less What is the relationship between spore morphology (specifi- obvious cases, as when a newly discovered epigeous species cally, ornamentation), dispersal, and symbiosis, and why does also lacks sterigmata capable of ballistospore discharge; ani- sporocarp size give a clue to nutritional mode? The ectomy- mal dispersal becomes an obvious hypothesis (Desjardin et al., corrhizal symbiosis has evolved at least 66 times (Tedersoo 2011). But for the majority of spore and sporocarp morpholo- et al., 2010; Tedersoo and Smith, 2013), likely from decom- gies, adaptive significance is unknown. Moreover, we do not poser ancestors in each case. Understanding these transitions know how spore features may or may not relate to a plethora is a major focus of mycology (Hibbett et al., 2000; Bruns and of other ecological strategies e including, for example, does Shefferson, 2004; Wolfe et al., 2012; Kohler et al., 2015). To 214 A. Pringle et al. date research has emphasized the genetics underpinning the have thought about water. We do know that water can move evolution to symbiosis, and the evolved interaction at the spores: one particularly elegant experiment involved Lyco- interface of a fungus and plant (Plett and Martin, 2011; Martin perdon perlatum, Fuligo septica, and yeast. Spores of all species and Kohler, 2014; Liao et al., 2014). But the emergence of an were moved from water in a Petri dish up an inclined glass ectomycorrhizal symbiosis may well involve correlated plane to heights of more than 20 cm (Bandoni and Koske, changes in spore or sporocarp morphology, for example, per- 1974); spores moved up the plane in response to a slow haps a transition to ornamented spores (Halbwachs et al., trickle of water (analogous to rain) that reached and perturbed 2015). the airewater interface in the dish. There is also no doubt that However, to our knowledge there is no research on the water moves species differently, for example, when water is origins of ornamentation, nor do we know if a reversal from poured over soil Penicillium spores do not move well while ornamented to smooth spores has happened in evolutionary spores of Zygorhynchus vuillemini (now Mucor moelleri) move history. The critical question is whether or not there is a easily (Burges, 1950). But as with insects, we have a limited fundamental difference in the habitats of saprotrophic and understanding of how effective water is as a vector through ectomycorrhizal fungi, so that each group requires a funda- soil, nor do we really understand potential interactions mentally different dispersal syndrome. Halbwachs et al. (2015) between water and ornamentation. suggest that the predominance of ornamented spores Perhaps ornamentation facilitates movement by animals, amongst ectomycorrhizal fungi is related to the fact that their but inhibits dispersal by water, and perhaps ECM of shallow primary resource (plant roots) is buried within the soil matrix, soils benefit from large, ornamented spores, while ECM rather than exposed as are most resources of saprotrophic associated with deep roots benefit from possession of small, fungi. Ornamentation, they hypothesize, may facilitate zoo- smooth spores. This kind of mechanism would help explain or chory by soil invertebrates that would carry the spores closer reinforce the strong patterns of vertical zonation seen in to their destination. Lilleskov and Bruns (2005) showed that many soil fungal communities (Dickie et al., 2002; Taylor et al., the knobby spores of the ectomycorrhizal fungus Tomentella 2014). Perhaps in some cases the depth of a species’ habitat is sublilacina were effectively dispersed on the body of mites, so more of an influence on morphology than trophic status. this is a plausible contention. But it is a single example, and In some cases, literature outside of mycology proves use- we do not know the answers to questions including, is T. ful. For example, the dispersal of bacteria through soil has also sublilacina representative of all ectomycorrhizal species, and been an active area of research. Cell size clearly plays a role in do unornamented spores NOT cling to invertebrates? Do these bacterial dispersal by water; smaller bacteria move more mites really carry the spores from the surface to deeper layers easily with water (Gannon et al., 1991) but soil properties, of soil? However, Halbwachs et al.’s ideas can be tested with specifically the size of the spaces or pores within soil, also experiments, for example to see whether smooth spores are influence migration (Huysman and Verstraete, 1993). Hydro- less effectively dispersed through soil by animals, and phobic bacteria move two to three times more slowly than whether animal dispersal does indeed help move ectomy- hydrophilic strains, because hydrophobic strains stick to soil corrhizal spores deeper into the soil column or closer to host particles (Huysman and Verstraete, 1993). Perhaps hydrophilic roots. fungal spores will also move more easily than hydrophobic The hypothesis linking ectomycorrhizal spore orna- fungal spores and, because fungal spores are often coated mentation to animal dispersal is just one of many plausible with numerous hydrophobic proteins, termed hydrophobins conjectures, and for example, the authors might as easily (Whiteford and Spanu, 2002), the potential for species to 20 A B 0.06 C 0.05 15 0.04 10 0.03 0.02 Dry weight (g) Dry weight Cap diameter (cm) diameter Cap 5 51015 0.01 Proportion of Proportion spores at 50cm 0 0.00 51015 51015202530 246810 Cap diameter (cm) Cap height (cm) Cap height (cm) Fig 1 e Allometric relationships between sporocarp characteristics of ectomycorrhizal fungi. Data are measurements made from 69 sporocarps of 15 species collected at Point Reyes National Seashore by KGP during 2008e2009. Each species is represented by a unique symbol. (A) Relationship between cap diameter and total dry weight.
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